Epigenetics and the placenta

Human Reproduction Update

Volumn 17, Issue 3, 2011, Pages 397-417

  Nelissen, Ewka C M ^a   van Montfoort, Aafke P A ^a   Dumoulin, John C M ^a   Evers, Johannes L H ^a  

^a MAASTRICHT UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

Environmental effects; Epigenetics; Genomic imprinting; Placenta

Indexed keywords

ALCOHOL; RNA;

ARTICLE; DNA METHYLATION; ENVIRONMENTAL FACTOR; EPIGENETICS; FETUS DEVELOPMENT; GENE EXPRESSION; GENOME IMPRINTING; HISTONE MODIFICATION; HUMAN; INTRAUTERINE GROWTH RETARDATION; NONHUMAN; OXYGEN TENSION; PATHOGENESIS; PLACENTA; PLACENTA DEVELOPMENT; PREECLAMPSIA; PREGNANCY; PRIORITY JOURNAL; REPRODUCTION; SMALL FOR DATE INFANT;

DNA METHYLATION; ENVIRONMENT; EPIGENESIS, GENETIC; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENOMIC IMPRINTING; HISTONES; HUMANS; MATERNAL EXPOSURE; PLACENTA; PLACENTA DISEASES; PREGNANCY; RNA, UNTRANSLATED;

EID: 79954463273     PISSN: 13554786     EISSN: 14602369     Source Type: Journal    
DOI: 10.1093/humupd/dmq052     Document Type: Article

References (216)

1. Adelman DM, Maltepe E, Simon MC. Multilineage embryonic hematopoiesis requires hypoxic ARNT activity. Genes Dev 1999;13:2478-2483.
2. Alsat E, Guibourdenche J, Couturier A, Evain-Brion D. Physiological role of human placental growth hormone. Mol Cell Endocrinol 1998;140:121-127.
3. Anderson MG, Nakane M, Ruan X, Kroeger PE, Wu-Wong JR. Expression of VDR and CYP24A1 mRNA in human tumors. Cancer Chemother Pharmacol 2006; 57:234-240.
4. Angiolini E, Fowden A, Coan P, Sandovici I, Smith P, Dean W, Burton G, Tycko B, Reik W, Sibley C. et al. Regulation of placental efficiency for nutrient transport by imprinted genes. Placenta 2006;27:S98-102.
5. Apostolidou S, Abu-Amero S, O'Donoghue K, Frost J, Olafsdottir O, Chavele KM, Whittaker JC, Loughna P, Stanier P, Moore GE. Elevated placental expression of the imprinted PHLDA2 gene is associated with low birth weight. J Mol Med 2007; 85:379-387.
6. Arima T, Hata K, Tanaka S, Kusumi M, Li E, Kato K, Shiota K, Sasaki H, Wake N. Loss of the maternal imprint in Dnmt3Lmat-/- mice leads to a differentiation defect in the extraembryonic tissue. Dev Biol 2006;297:361-373.
7. Baccarelli A, Bollati V. Epigenetics and environmental chemicals. Curr Opin Pediatr 2009;21:243-251.
8. Bamberg C, Kalache KD. Prenatal diagnosis of fetal growth restriction. Semin Fetal Neonatal Med 2004;9:387-394.
9. Bao S, Obata Y, Carroll J, Domeki I, Kono T. Epigenetic modifications necessary for normal development are established during oocyte growth in mice. Biol Reprod 2000;62:616-621.
10. Barad O, Meiri E, Avniel A, Aharonov R, Barzilai A, Bentwich I, Einav U, Gilad S, Hurban P, Karov Y. et al. MicroRNA expression detected by oligonucleotide microarrays: system establishment and expression profiling in human tissues. Genome Res 2004;14:2486-2494.
11. Barker DJ, Hales CN, Fall CH, Osmond C, Phipps K, Clark PM. Type 2 (non-insulin-dependent) diabetes mellitus, hypertension and hyperlipidaemia (syndrome X): relation to reduced fetal growth. Diabetologia 1993;36:62-67.
12. Barlow DP. Methylation and imprinting: from host defense to gene regulation? Science 1993;260:309-310.
13. Barton SC, Surani MA, Norris ML. Role of paternal and maternal genomes in mouse development. Nature 1984;311:374-376.
14. Beaujean N, Hartshorne G, Cavilla J, Taylor J, Gardner J, Wilmut I, Meehan R, Young L. Non-conservation of mammalian preimplantation methylation dynamics. Curr Biol 2004;14:R266-267.
15. Bird A. DNA methylation patterns and epigenetic memory. Genes Dev 2002; 16:6-21.
16. Bird A. Perceptions of epigenetics. Nature 2007;447:396-398.
17. Bodnar LM, Catov JM, Simhan HN, Holick MF, Powers RW, Roberts JM. Maternal vitamin D deficiency increases the risk of preeclampsia. J Clin Endocrinol Metab 2007;92:3517-3522.
18. Bourc'his D, Bestor TH. Meiotic catastrophe and retrotransposon reactivation in male germ cells lacking Dnmt3L. Nature 2004;431:96-99.
19. Bourc'his D, Xu GL, Lin CS, Bollman B, Bestor TH. Dnmt3L and the establishment of maternal genomic imprints. Science 2001;294:2536-2539.
20. Boyer LA, Plath K, Zeitlinger J, Brambrink T, Medeiros LA, Lee TI, Levine SS, Wernig M, Tajonar A, Ray MK. et al. Polycomb complexes repress developmental regulators in murine embryonic stem cells. Nature 2006; 441:349-353.
21. Boyko EJ. Proportion of type 2 diabetes cases resulting from impaired fetal growth. Diabetes Care 2000;23:1260-1264.
22. Bromer JG, Wu J, Zhou Y, Taylor HS. Hypermethylation of homeobox A10 by in utero diethylstilbestrol exposure: an epigenetic mechanism for altered developmental programming. Endocrinology 2009;150:3376-3382.
23. Buiting K, Saitoh S, Gross S, Dittrich B, Schwartz S, Nicholls RD, Horsthemke B. Inherited microdeletions in the Angelman and Prader-Willi syndromes define an imprinting centre on human chromosome 15. Nat Genet 1995;9:395-400.
24. Carninci P, Kasukawa T, Katayama S, Gough J, Frith MC, Maeda N, Oyama R, Ravasi T, Lenhard B, Wells C. et al. The transcriptional landscape of the mammalian genome. Science 2005;309:1559-1563.
25. Chaddha V, Viero S, Huppertz B, Kingdom J. Developmental biology of the placenta and the origins of placental insufficiency. Semin Fetal Neonatal Med 2004;9:357-369.
26. Chapman V, Forrester L, Sanford J, Hastie N, Rossant J. Cell lineage-specific undermethylation of mouse repetitive DNA. Nature 1984;307:284-286.
27. Charalambous M, da Rocha ST, Ferguson-Smith AC. Genomic imprinting, growth control and the allocation of nutritional resources: consequences for postnatal life. Curr Opin Endocrinol Diabetes Obes 2007;14:3-12.
28. Chelbi ST, Vaiman D. Genetic and epigenetic factors contribute to the onset of preeclampsia. Mol Cell Endocrinol 2008;282:120-129.
29. Chelbi ST, Mondon F, Jammes H, Buffat C, Mignot TM, Tost J, Busato F, Gut I, Rebourcet R, Laissue P. et al. Expressional and epigenetic alterations of placental serine protease inhibitors: SERPINA3 is a potential marker of preeclampsia. Hypertension 2007;49:76-83.
30. Chiu RW, Chim SS, Wong IH, Wong CS, Lee WS, To KF, Tong JH, Yuen RK, Shum AS, Chan JK. et al. Hypermethylation of RASSF1A in human and rhesus placentas. Am J Pathol 2007;170:941-950.
31. Chuang HC, Chang CW, Chang GD, Yao TP, Chen H. Histone deacetylase 3 binds to and regulates the GCMa transcription factor. Nucleic Acids Res 2006;34:1459-1469.
32. Coan PM, Burton GJ, Ferguson-Smith AC. Imprinted genes in the placenta-a review. Placenta 2005;26:S10-20.
33. Coan PM, Fowden AL, Constancia M, Ferguson-Smith AC, Burton GJ, Sibley CP. Disproportional effects of Igf2 knockout on placental morphology and diffusional exchange characteristics in the mouse. J Physiol 2008;586:5023-5032.
34. Constancia M, Hemberger M, Hughes J, Dean W, Ferguson-Smith A, Fundele R, Stewart F, Kelsey G, Fowden A, Sibley C. et al. Placental-specific IGF-II is a major modulator of placental and fetal growth. Nature 2002;417:945-948.
35. Cox GF, Burger J, Lip V, Mau UA, Sperling K, Wu BL, Horsthemke B. Intracytoplasmic sperm injection may increase the risk of imprinting defects. Am J Hum Genet 2002;71:162-164.
36. Cross JC. The genetics of pre-eclampsia: a feto-placental or maternal problem? Clin Genet 2003;64:96-103.
37. Curhan GC, Chertow GM, Willett WC, Spiegelman D, Colditz GA, Manson JE, Speizer FE, Stampfer MJ. Birth weight and adult hypertension and obesity in women. Circulation 1996a;94:1310-1315.
38. Curhan GC, Willett WC, Rimm EB, Spiegelman D, Ascherio AL, Stampfer MJ. Birth weight and adult hypertension, diabetes mellitus, and obesity in US men. Circulation 1996b;94:3246-3250.
39. DeBaun MR, Niemitz EL, Feinberg AP. Association of in vitro fertilization with Beckwith-Wiedemann syndrome and epigenetic alterations of LIT1 and H19. Am J Hum Genet 2003;72:156-160.
40. Delcuve GP, Rastegar M, Davie JR. Epigenetic control. J Cell Physiol 2009;219:243-250.
41. DeLuca HF. Overview of general physiologic features and functions of vitamin D. Am J Clin Nutr 2004;80:1689S-1696S.
42. Devriendt K. Hydatidiform mole and triploidy: the role of genomic imprinting in placental development. Hum Reprod Update 2005;11:137-142.
43. Diplas AI, Lambertini L, Lee MJ, Sperling R, Lee YL, Wetmur J, Chen J. Differential expression of imprinted genes in normal and IUGR human placentas. Epigenetics 2009;4:235-240.
44. Doherty AS, Mann MR, Tremblay KD, Bartolomei MS, Schultz RM. Differential effects of culture on imprinted H19 expression in the preimplantation mouse embryo. Biol Reprod 2000;62:1526-1535.
45. Dokras A, Coffin J, Field L, Frakes A, Lee H, Madan A, Nelson T, Ryu GY, Yoon JG, Madan A. Epigenetic regulation of maspin expression in the human placenta. Mol Hum Reprod 2006;12:611-617.
46. Donker RB, Mouillet JF, Nelson DM, Sadovsky Y. The expression of Argonaute2 and related microRNA biogenesis proteins in normal and hypoxic trophoblasts. Mol Hum Reprod 2007;13:273-279.
47. Dumoulin JC, Land JA, Van Montfoort AP, Nelissen EC, Coonen E, Derhaag JG, Schreurs IL, Dunselman GA, Kester AD, Geraedts JP. et al. Effect of in vitro culture of human embryos on birthweight of newborns. Hum Reprod 2010; 25:605-612.
48. Dusso AS, Brown AJ, Slatopolsky E. Vitamin D. Am J Physiol Renal Physiol 2005; 289:F8-28.
49. Edwards CA, Ferguson-Smith AC. Mechanisms regulating imprinted genes in clusters. Curr Opin Cell Biol 2007;19:281-289.
50. Engstrom PG, Suzuki H, Ninomiya N, Akalin A, Sessa L, Lavorgna G, Brozzi A, Luzi L, Tan SL, Yang L. et al. Complex Loci in human and mouse genomes. PLoS Genet 2006;2:e47.
51. Eriksson JG, Forsen TJ, Osmond C, Barker DJ. Pathways of infant and childhood growth that lead to type 2 diabetes. Diabetes Care 2003;26:3006-3010.
52. Ertzeid G, Storeng R. Adverse effects of gonadotrophin treatment on pre- and postimplantation development in mice. J Reprod Fertil 1992;96:649-655.
53. Ertzeid G, Storeng R. The impact of ovarian stimulation on implantation and fetal development in mice. Hum Reprod 2001;16:221-225.
54. Esteve PO, Chin HG, Smallwood A, Feehery GR, Gangisetty O, Karpf AR, Carey MF, Pradhan S. Direct interaction between DNMT1 and G9a coordinates DNA and histone methylation during replication. Genes Dev 2006; 20:3089-3103.
55. Fauque P, Jouannet P, Lesaffre C, Ripoche MA, Dandolo L, Vaiman D, Jammes H. Assisted Reproductive Technology affects developmental kinetics, H19 Imprinting Control Region methylation and H19 gene expression in individual mouse embryos. BMC Dev Biol 2007;7:116.
56. Fauque P, Mondon F, Letourneur F, Ripoche MA, Journot L, Barbaux S, Dandolo L, Patrat C, Wolf JP, Jouannet P. et al. In vitro fertilization and embryo culture strongly impact the placental transcriptome in the mouse model. PLoS One 2010;5:e9218.
57. Feil R. Environmental and nutritional effects on the epigenetic regulation of genes. Mutat Res 2006;600:46-57.
58. Ferguson-Smith AC, Moore T, Detmar J, Lewis A, Hemberger M, Jammes H, Kelsey G, Roberts CT, Jones H, Constancia M. Epigenetics and imprinting of the trophoblast-a workshop report. Placenta 2006;27:S122-126.
59. Ferretti C, Bruni L, Dangles-Marie V, Pecking AP, Bellet D. Molecular circuits shared by placental and cancer cells, and their implications in the proliferative, invasive and migratory capacities of trophoblasts. Hum Reprod Update 2007;13:121-141.
60. Fisher SJ. The placental problem: linking abnormal cytotrophoblast differentiation to the maternal symptoms of preeclampsia. Reprod Biol Endocrinol 2004;2:53.
61. Fortier AL, Lopes FL, Darricarrere N, Martel J, Trasler JM. Superovulation alters the expression of imprinted genes in the midgestation mouse placenta. Hum Mol Genet 2008;17:1653-1665.
62. Fossum GT, Davidson A, Paulson RJ. Ovarian hyperstimulation inhibits embryo implantation in the mouse. J In Vitro Fert Embryo Transf 1989;6:7-10.
63. Fowden AL, Sibley C, Reik W, Constancia M. Imprinted genes, placental development and fetal growth. Horm Res 2006;65:50-58.
64. Frank D, Fortino W, Clark L, Musalo R, Wang W, Saxena A, Li CM, Reik W, Ludwig T, Tycko B. Placental overgrowth in mice lacking the imprinted gene Ipl. Proc Natl Acad Sci USA 2002;99:7490-7495.
65. Gicquel C, Gaston V, Mandelbaum J, Siffroi JP, Flahault A, Le Bouc Y. In vitro fertilization may increase the risk of Beckwith-Wiedemann syndrome related to the abnormal imprinting of the KCN1OT gene. Am J Hum Genet 2003;72:1338-1341.
66. Gluckman PD, Hanson MA. Maternal constraint of fetal growth and its consequences. Semin Fetal Neonatal Med 2004;9:419-425.
67. Gomes MV, Huber J, Ferriani RA, Amaral Neto AM, Ramos ES. Abnormal methylation at the KvDMR1 imprinting control region in clinically normal children conceived by assisted reproductive technologies. Mol Hum Reprod 2009;15:471-477.
68. Guillemot F, Nagy A, Auerbach A, Rossant J, Joyner AL. Essential role of Mash-2 in extraembryonic development. Nature 1994;371: 333-336.
69. Guo L, Choufani S, Ferreira J, Smith A, Chitayat D, Shuman C, Uxa R, Keating S, Kingdom J, Weksberg R. Altered gene expression and methylation of the human chromosome 11 imprinted region in small for gestational age (SGA) placentae. Dev Biol 2008;320:79-91.
70. Haig D. Genomic imprinting and kinship: how good is the evidence? Annu Rev Genet 2004;38:553-585.
71. Halliday J, Oke K, Breheny S, Algar E, Amor DJ. Beckwith-Wiedemann syndrome and IVF: a case-control study. Am J Hum Genet 2004;75:526-528.
72. Hansen M, Bower C, Milne E, de Klerk N, Kurinczuk JJ. Assisted reproductive technologies and the risk of birth defects-a systematic review. Hum Reprod 2005;20:328-338.
73. Hata K, Okano M, Lei H, Li E. Dnmt3L cooperates with the Dnmt3 family of de novo DNA methyltransferases to establish maternal imprints in mice. Development 2002;129:1983-1993.
74. Haycock PC, Ramsay M. Exposure of mouse embryos to ethanol during preimplantation development: effect on DNA methylation in the h19 imprinting control region. Biol Reprod 2009;81:618-627.
75. Heikkila A, Tuomisto T, Hakkinen SK, Keski-Nisula L, Heinonen S, Yla-Herttuala S. Tumor suppressor and growth regulatory genes are overexpressed in severe early-onset preeclampsia-an array study on case-specific human preeclamptic placental tissue. Acta Obstet Gynecol Scand 2005;84:679-689.
76. Helmerhorst FM, Perquin DA, Donker D, Keirse MJ. Perinatal outcome of singletons and twins after assisted conception: a systematic review of controlled studies. Br Med J 2004;328:261.
77. Hemberger M. Epigenetic landscape required for placental development. Cell Mol Life Sci 2007;64:2422-2436.
78. Herman JG, Baylin SB. Gene silencing in cancer in association with promoter hypermethylation. N Engl J Med 2003;349:2042-2054.
79. Horsthemke B, Ludwig M. Assisted reproduction: the epigenetic perspective. Hum Reprod Update 2005;11:473-482.
80. Hui P, Martel M, Parkash V. Gestational trophoblastic diseases: recent advances in histopathologic diagnosis and related genetic aspects. Adv Anat Pathol 2005; 12:116-125.
81. Jackson RA, Gibson KA, Wu YW, Croughan MS. Perinatal outcomes in singletons following in vitro fertilization: a meta-analysis. Obstet Gynecol 2004;103:551-563.
82. Januchowski R, Dabrowski M, Ofori H, Jagodzinski PP. Trichostatin A down-regulate DNA methyltransferase 1 in Jurkat T cells. Cancer Lett 2007;246:313-317.
83. Jirtle RL, Skinner MK. Environmental epigenomics and disease susceptibility. Nat Rev Genet 2007;8:253-262.
84. Kagami M, Nagai T, Fukami M, Yamazawa K, Ogata T. Silver-Russell syndrome in a girl born after in vitro fertilization: partial hypermethylation at the differentially methylated region of PEG1/MEST. J Assist Reprod Genet 2007;24:131-136.
85. Kanayama N, Takahashi K, Matsuura T, Sugimura M, Kobayashi T, Moniwa N, Tomita M, Nakayama K. Deficiency in p57Kip2 expression induces preeclampsia-like symptoms in mice. Mol Hum Reprod 2002;8:1129-1135.
86. Kaneda M, Okano M, Hata K, Sado T, Tsujimoto N, Li E, Sasaki H. Essential role for de novo DNA methyltransferase Dnmt3a in paternal and maternal imprinting. Nature 2004;429:900-903.
87. Kaneko-Ishino T, Kohda T, Ishino F. The regulation and biological significance of genomic imprinting in mammals. J Biochem 2003;133:699-711.
88. Katari S, Turan N, Bibikova M, Erinle O, Chalian R, Foster M, Gaughan JP, Coutifaris C, Sapienza C. DNA methylation and gene expression differences in children conceived in vitro or in vivo. Hum Mol Genet 2009;18:3769-3778.
89. Katayama S, Tomaru Y, Kasukawa T,Waki K, Nakanishi M, Nakamura M, Nishida H, Yap CC, Suzuki M, Kawai J. et al. Antisense transcription in the mammalian transcriptome. Science 2005;309:1564-1566.
90. Khosla S, Dean W, Brown D, Reik W, Feil R. Culture of preimplantation mouse embryos affects fetal development and the expression of imprinted genes. Biol Reprod 2001;64:918-926.
91. Kim SJ, Park SE, Lee C, Lee SY, Kim IH, An HJ, Oh YK. Altered imprinting, promoter usage, and expression of insulin-like growth factor-II gene in gestational trophoblastic diseases. Gynecol Oncol 2003;88:411-418.
92. Kimura AP, Liebhaber SA, Cooke NE. Epigenetic modifications at the human growth hormone locus predict distinct roles for histone acetylation and methylation in placental gene activation. Mol Endocrinol 2004;18:1018-1032.
93. Koerner MV, Pauler FM, Huang R, Barlow DP. The function of non-coding RNAs in genomic imprinting. Development 2009;136:1771-1783.
94. Kono T, Obata Y, Wu Q, Niwa K, Ono Y, Yamamoto Y, Park ES, Seo JS, Ogawa H. Birth of parthenogenetic mice that can develop to adulthood. Nature 2004; 428:860-864.
95. Koslowski M, Sahin U, Mitnacht-Kraus R, Seitz G, Huber C, Tureci O. A placenta-specific gene ectopically activated in many human cancers is essentially involved in malignant cell processes. Cancer Res 2007;67:9528-9534.
96. Kovacic B, Vlaisavljevic V. Influence of atmospheric versus reduced oxygen concentration on development of human blastocysts in vitro: a prospective study on sibling oocytes. Reprod Biomed Online 2008;17:229-236.
97. Laird PW. The power and the promise of DNA methylation markers. Nat Rev Cancer 2003;3:253-266.
98. Lambertini L, Diplas AI, Lee MJ, Sperling R, Chen J, Wetmur J. A sensitive functional assay reveals frequent loss of genomic imprinting in human placenta. Epigenetics 2008;3:261-269.
99. Lee J, Inoue K, Ono R, Ogonuki N, Kohda T, Kaneko-Ishino T, Ogura A, Ishino F. Erasing genomic imprinting memory in mouse clone embryos produced from day 11.5 primordial germ cells. Development 2002;129:1807-1817.
100. Lee TI, Jenner RG, Boyer LA, Guenther MG, Levine SS, Kumar RM, Chevalier B, Johnstone SE, Cole MF, Isono K. et al. Control of developmental regulators by Polycomb in human embryonic stem cells. Cell 2006;125:301-313.
101. Lefebvre L, Viville S, Barton SC, Ishino F, Keverne EB, Surani MA. Abnormal maternal behaviour and growth retardation associated with loss of the imprinted gene Mest. Nat Genet 1998;20:163-169.
102. Lehnertz B, Ueda Y, Derijck AA, Braunschweig U, Perez-Burgos L, Kubicek S, Chen T, Li E, Jenuwein T, Peters AH. Suv39h-mediated histone H3 lysine 9 methylation directs DNA methylation to major satellite repeats at pericentric heterochromatin. Curr Biol 2003;13:1192-1200.
103. Lewis A, Mitsuya K, Umlauf D, Smith P, Dean W, Walter J, Higgins M, Feil R, Reik W. Imprinting on distal chromosome 7 in the placenta involves repressive histone methylation independent of DNA methylation. Nat Genet 2004; 36:1291-1295.
104. Li E, Bestor TH, Jaenisch R. Targeted mutation of the DNA methyltransferase gene results in embryonic lethality. Cell 1992;69:915-926.
105. Li HW, Tsao SW, Cheung AN. Current understandings of the molecular genetics of gestational trophoblastic diseases. Placenta 2002;23:20-31.
106. Li S, Hursting SD, Davis BJ, McLachlan JA, Barrett JC. Environmental exposure, DNA methylation, and gene regulation: lessons from diethylstilbesterol-induced cancers. Ann N Y Acad Sci 2003;983:161-169.
107. Lie RT, Lyngstadaas A, Orstavik KH, Bakketeig LS, Jacobsen G, Tanbo T. Birth defects in children conceived by ICSI compared with children conceived by other IVF-methods; a meta-analysis. Int J Epidemiol 2005;34:696-701.
108. Lucifero D, Chaillet JR, Trasler JM. Potential significance of genomic imprinting defects for reproduction and assisted reproductive technology. Hum Reprod Update 2004a;10:3-18.
109. Lucifero D, Mann MR, Bartolomei MS, Trasler JM. Gene-specific timing and epigenetic memory in oocyte imprinting. Hum Mol Genet 2004b;13:839-849.
110. Maher ER, Brueton LA, Bowdin SC, Luharia A, Cooper W, Cole TR, Macdonald F, Sampson JR, Barratt CL, Reik W. et al. Beckwith-Wiedemann syndrome and assisted reproduction technology (ART). J Med Genet 2003;40:62-64.
111. Maltepe E, Krampitz GW, Okazaki KM, Red-Horse K, Mak W, Simon MC, Fisher SJ. Hypoxia-inducible factor-dependent histone deacetylase activity determines stem cell fate in the placenta. Development 2005;132:3393-3403.
112. Mancini-Dinardo D, Steele SJ, Levorse JM, Ingram RS, Tilghman SM. Elongation of the Kcnq1ot1 transcript is required for genomic imprinting of neighboring genes. Genes Dev 2006;20:1268-1282.
113. Manes C, Menzel P. Demethylation of CpG sites in DNA of early rabbit trophoblast. Nature 1981;293:589-590.
114. Mann MR, Lee SS, Doherty AS, Verona RI, Nolen LD, Schultz RM, Bartolomei MS. Selective loss of imprinting in the placenta following preimplantation development in culture. Development 2004;131:3727-3735.
115. Market-Velker BA, Zhang L, Magri LS, Bonvissuto AC, Mann MR. Dual effects of superovulation: loss of maternal and paternal imprinted methylation in a dose-dependent manner. Hum Mol Genet 2010;19:36-51.
116. Maulik D. Fetal growth compromise: definitions, standards, and classification. Clin Obstet Gynecol 2006;49:214-218.
117. Mayer W, Niveleau A, Walter J, Fundele R, Haaf T. Demethylation of the zygotic paternal genome. Nature 2000;403:501-502.
118. McGovern PG, Llorens AJ, Skurnick JH, Weiss G, Goldsmith LT. Increased risk of preterm birth in singleton pregnancies resulting from in vitro fertilization-embryo transfer or gamete intrafallopian transfer: a meta-analysis. Fertil Steril 2004;82:1514-1520.
119. McGrath J, Solter D. Completion of mouse embryogenesis requires both the maternal and paternal genomes. Cell 1984;37:179-183.
120. McMinn J, Wei M, Schupf N, Cusmai J, Johnson EB, Smith AC, Weksberg R, Thaker HM, Tycko B. Unbalanced placental expression of imprinted genes in human intrauterine growth restriction. Placenta 2006;27:540-549.
121. Meintjes M, Chantilis SJ, Douglas JD, Rodriguez AJ, Guerami AR, Bookout DM, Barnett BD, Madden JD. A controlled randomized trial evaluating the effect of lowered incubator oxygen tension on live births in a predominantly blastocyst transfer program. Hum Reprod 2009;24:300-307.
122. Miri K, Varmuza S. Imprinting and extraembryonic tissues-mom takes control. Int Rev Cell Mol Biol 2009;276:215-262.
123. Monk D, Moore GE. Intrauterine growth restriction-genetic causes and consequences. Semin Fetal Neonatal Med 2004;9:371-378.
124. Monk D, Arnaud P, Apostolidou S, Hills FA, Kelsey G, Stanier P, Feil R, Moore GE. Limited evolutionary conservation of imprinting in the human placenta. Proc Natl Acad Sci USA 2006;103:6623-6628.
125. Moore T, Haig D. Genomic imprinting in mammalian development: a parental tug-of-war. Trends Genet 1991;7:45-49.
126. Morison IM, Reeve AE. A catalogue of imprinted genes and parent-of-origin effects in humans and animals. Hum Mol Genet 1998;7:1599-1609.
127. Niessen HE, Demmers JA, Voncken JW. Talking to chromatin: post-translational modulation of polycomb group function. Epigenetics Chromatin 2009;2:10.
128. Novakovic B, Rakyan V, Ng HK, Manuelpillai U, Dewi C, Wong NC, Morley R, Down T, Beck S, Craig JM. et al. Specific tumour-associated methylation in normal human term placenta and first-trimester cytotrophoblasts. Mol Hum Reprod 2008;14:547-554.
129. Novakovic B, Sibson M, Ng HK, Manuelpillai U, Rakyan V, Down T, Beck S, Fournier T, Evain-Brion D, Dimitriadis E. et al. Placenta-specific methylation of the vitamin D 24-hydroxylase gene: implications for feedback autoregulation of active vitamin D levels at the fetomaternal interface. J Biol Chem 2009; 284:14838-14848.
130. O'Carroll D, Erhardt S, Pagani M, Barton SC, Surani MA, Jenuwein T. The polycomb-group gene Ezh2 is required for early mouse development. Mol Cell Biol 2001;21:4330-4336.
131. Obata Y, Kono T. Maternal primary imprinting is established at a specific time for each gene throughout oocyte growth. J Biol Chem 2002;277:5285-5289.
132. Okano M, Xie S, Li E. Cloning and characterization of a family of novel mammalian DNA (cytosine-5) methyltransferases. Nat Genet 1998;19:219-220.
133. Okano M, Bell DW, Haber DA, Li E. DNA methyltransferases Dnmt3a and Dnmt3b are essential for de novo methylation and mammalian development. Cell 1999; 99:247-257.
134. Okazaki Y, Furuno M, Kasukawa T, Adachi J, Bono H, Kondo S, Nikaido I, Osato N, Saito R, Suzuki H. et al. Analysis of the mouse transcriptome based on functional annotation of 60,770 full-length cDNAs. Nature 2002;420:563-573.
135. Ono R, Nakamura K, Inoue K, Naruse M, Usami T, Wakisaka-Saito N, Hino T, Suzuki-Migishima R, Ogonuki N, Miki H. et al. Deletion of Peg10, an imprinted gene acquired from a retrotransposon, causes early embryonic lethality. Nat Genet 2006;38:101-106.
136. Oudejans CB, Mulders J, Lachmeijer AM, van Dijk M, Konst AA, Westerman BA, van Wijk IJ, Leegwater PA, Kato HD, Matsuda T. et al. The parent-of-origin effect of 10q22 in pre-eclamptic females coincides with two regions clustered for genes with down-regulated expression in androgenetic placentas. Mol Hum Reprod 2004;10:589-598.
137. Pandey RR, Mondal T, Mohammad F, Enroth S, Redrup L, Komorowski J, Nagano T, Mancini-Dinardo D, Kanduri C. Kcnq1ot1 antisense noncoding RNA mediates lineage-specific transcriptional silencing through chromatin-level regulation. Mol Cell 2008;32:232-246.
138. Pasini D, Bracken AP, Jensen MR, Lazzerini Denchi E, Helin K. Suz12 is essential for mouse development and for EZH2 histone methyltransferase activity. Embo J 2004;23:4061-4071.
139. Pauler FM, Koerner MV, Barlow DP. Silencing by imprinted noncoding RNAs: is transcription the answer? Trends Genet 2007;23:284-292.
140. Peterson CL, Laniel MA. Histones and histone modifications. Curr Biol 2004; 14:R546-551.
141. Pidoux G, Gerbaud P, Laurendeau I, Guibourdenche J, Bertin G, Vidaud M, Evain-Brion D, Frendo JL. Large variability of trophoblast gene expression within and between human normal term placentae. Placenta 2004;25:469-473.
142. Pineles BL, Romero R, Montenegro D, Tarca AL, Han YM, Kim YM, Draghici S, Espinoza J, Kusanovic JP, Mittal P. et al. Distinct subsets of microRNAs are expressed differentially in the human placentas of patients with preeclampsia. Am J Obstet Gynecol 2007;196:e261-266.
143. Piras G, El Kharroubi A, Kozlov S, Escalante-Alcalde D, Hernandez L, Copeland NG, Gilbert DJ, Jenkins NA, Stewart CL. Zac1 (Lot1), a potential tumor suppressor gene, and the gene for epsilon-sarcoglycan are maternally imprinted genes: identification by a subtractive screen of novel uniparental fibroblast lines. Mol Cell Biol 2000;20:3308-3315.
144. Pozharny Y, Lambertini L, Ma Y, Ferrara L, Litton CG, Diplas A, Jacobs AR, Chen J, Stone JL, Wetmur J. et al. Genomic loss of imprinting in first-trimester human placenta. Am J Obstet Gynecol 2010;202:e391-398.
145. Rahnama F, Shafiei F, Gluckman PD, Mitchell MD, Lobie PE. Epigenetic regulation of human trophoblastic cell migration and invasion. Endocrinology 2006; 147:5275-5283.
146. Reik W. Stability and flexibility of epigenetic gene regulation in mammalian development. Nature 2007;447:425-432.
147. Reik W, Walter J. Genomic imprinting: parental influence on the genome. Nat Rev Genet 2001;2:21-32.
148. Reik W, Dean W, Walter J. Epigenetic reprogramming in mammalian development. Science 2001;293:1089-1093.
149. Reik W, Constancia M, Fowden A, Anderson N, Dean W, Ferguson-Smith A, Tycko B, Sibley C. Regulation of supply and demand for maternal nutrients in mammals by imprinted genes. J Physiol 2003a;547:35-44.
150. Reik W, Santos F, Mitsuya K, Morgan H, Dean W. Epigenetic asymmetry in the mammalian zygote and early embryo: relationship to lineage commitment? Philos Trans R Soc Lond B Biol Sci 2003b;358:1403-1409; discussion 1409.
151. Renfree MB, Ager EI, Shaw G, Pask AJ. Genomic imprinting in marsupial placentation. Reproduction 2008;136:523-531.
152. Rimm AA, Katayama AC, Diaz M, Katayama KP. A meta-analysis of controlled studies comparing major malformation rates in IVF and ICSI infants with naturally conceived children. J Assist Reprod Genet 2004;21:437-443.
153. Rinaudo PF, Giritharan G, Talbi S, Dobson AT, Schultz RM. Effects of oxygen tension on gene expression in preimplantation mouse embryos. Fertil Steril 2006; 86:1252-1265.
154. Rivera RM, Stein P, Weaver JR, Mager J, Schultz RM, Bartolomei MS. Manipulations of mouse embryos prior to implantation result in aberrant expression of imprinted genes on day 9.5 of development. Hum Mol Genet 2008;17:1-14.
155. Ross MG, Beall MH. Adult sequelae of intrauterine growth restriction. Semin Perinatol 2008;32:213-218.
156. Rossant J, Cross JC. Placental development: lessons from mouse mutants. Nat Rev Genet 2001;2:538-548.
157. Rossant J, Sanford JP, Chapman VM, Andrews GK. Undermethylation of structural gene sequences in extraembryonic lineages of the mouse. Dev Biol 1986; 117:567-573.
158. Royo H, Cavaille J. Non-coding RNAs in imprinted gene clusters. Biol Cell 2008; 100:149-166.
159. Russo VEA, Martienssen RA, Riggs AD. Epigenetic Mechanisms of Gene Regulation. Woodbury: Cold Spring Harbor Laboratory Press, 1996.
160. Salas M, John R, Saxena A, Barton S, Frank D, Fitzpatrick G, Higgins MJ, Tycko B. Placental growth retardation due to loss of imprinting of Phlda2. Mech Dev 2004;121:1199-1210.
161. Santos F, Hendrich B, Reik W, Dean W. Dynamic reprogramming of DNA methylation in the early mouse embryo. Dev Biol 2002;241:172-182.
162. Santos F, Zakhartchenko V, Stojkovic M, Peters A, Jenuwein T, Wolf E, Reik W, Dean W. Epigenetic marking correlates with developmental potential in cloned bovine preimplantation embryos. Curr Biol 2003;13:1116-1121.
163. Sasaki H, Ferguson-Smith AC, Shum AS, Barton SC, Surani MA. Temporal and spatial regulation of H19 imprinting in normal and uniparental mouse embryos. Development 1995;121:4195-4202.
164. Sato A, Otsu E, Negishi H, Utsunomiya T, Arima T. Aberrant DNA methylation of imprinted loci in superovulated oocytes. Hum Reprod 2007;22:26-35.
165. Sato K, Fukata H, Kogo Y, Ohgane J, Shiota K, Mori C. Neonatal exposure to diethylstilbestrol alters expression of DNA methyltransferases and methylation of genomic DNA in the mouse uterus. Endocr J 2009;56:131-139.
166. Seely EW. Calciotropic hormones in preeclampsia: a renewal of interest. J Clin Endocrinol Metab 2007;92:3402-3403.
167. Serman L, Vlahovic M, Sijan M, Bulic-Jakus F, Serman A, Sincic N, Matijevic R, Juric-Lekic G, Katusic A. The impact of 5-azacytidine on placental weight, glycoprotein pattern and proliferating cell nuclear antigen expression in rat placenta. Placenta 2007;28:803-811.
168. Shin JY, Fitzpatrick GV, Higgins MJ. Two distinct mechanisms of silencing by the KvDMR1 imprinting control region. Embo J 2008;27:168-178.
169. Sibley CP, Coan PM, Ferguson-Smith AC, Dean W, Hughes J, Smith P, Reik W, Burton GJ, Fowden AL, Constancia M. Placental-specific insulin-like growth factor 2 (Igf2) regulates the diffusional exchange characteristics of the mouse placenta. Proc Natl Acad Sci USA 2004;101:8204-8208.
170. Sims RJ 3rd, Reinberg D. Histone H3 Lys 4 methylation: caught in a bind. Genes Dev 2006;20:2779-2786.
171. Sinclair KD, Young LE, Wilmut I, McEvoy TG. In-utero overgrowth in ruminants following embryo culture: lessons from mice and a warning to men. Hum Reprod 2000;15:68-86.
172. Singh SM, Murphy B, O'Reilly RL. Involvement of gene-diet/drug interaction in DNA methylation and its contribution to complex diseases: from cancer to schizophrenia. Clin Genet 2003;64:451-460.
173. Sleutels F, Zwart R, Barlow DP. The non-coding Air RNA is required for silencing autosomal imprinted genes. Nature 2002;415:810-813.
174. Spahn L, Barlow DP. An ICE pattern crystallizes. Nat Genet 2003;35:11-12.
175. Steinhoff C, Paulsen M, Kielbasa S, Walter J, Vingron M. Expression profile and transcription factor binding site exploration of imprinted genes in human and mouse. BMC Genomics 2009;10:144.
176. Surani MA, Barton SC, Norris ML. Development of reconstituted mouse eggs suggests imprinting of the genome during gametogenesis. Nature 1984;308:548-550.
177. Swales AK, Spears N. Genomic imprinting and reproduction. Reproduction 2005; 130:389-399.
178. Takahashi K, Kobayashi T, Kanayama N. p57(Kip2) regulates the proper development of labyrinthine and spongiotrophoblasts. Mol Hum Reprod 2000;6:1019-1025.
179. Tanaka M, Puchyr M, Gertsenstein M, Harpal K, Jaenisch R, Rossant J, Nagy A. Parental origin-specific expression of Mash2 is established at the time of implantation with its imprinting mechanism highly resistant to genome-wide demethylation. Mech Dev 1999;87:129-142.
180. Terranova R, Yokobayashi S, Stadler MB, Otte AP, van Lohuizen M, Orkin SH, Peters AH. Polycomb group proteins Ezh2 and Rnf2 direct genomic contraction and imprinted repression in early mouse embryos. Dev Cell 2008;15:668-679.
181. Thompson JG, Gardner DK, Pugh PA, McMillan WH, Tervit HR. Lamb birth weight is affected by culture system utilized during in vitro pre-elongation development of ovine embryos. Biol Reprod 1995;53:1385-1391.
182. Tierling S, Souren NY, Gries J, Lo Porto C, Groth M, Lutsik P, Neitzel H, Utz-Billing I, Gillessen-Kaesbach G, Kentenich H. et al. Assisted reproductive technologies do not enhance the variability of DNA methylation imprints in human. J Med Genet 2010;47:371-76.
183. Torres-Padilla ME. Cell identity in the preimplantation mammalian embryo: an epigenetic perspective from the mouse. Hum Reprod 2008;23:1246-1252.
184. Torres-Padilla ME, Parfitt DE, Kouzarides T, Zernicka-Goetz M. Histone arginine methylation regulates pluripotency in the early mouse embryo. Nature 2007; 445:214-218.
185. Tremblay KD, Saam JR, Ingram RS, Tilghman SM, Bartolomei MS. A paternal-specific methylation imprint marks the alleles of the mouse H19 gene. Nat Genet 1995; 9:407-413.
186. Turner BM. Cellular memory and the histone code. Cell 2002;111:285-291.
187. Tycko B. Imprinted genes in placental growth and obstetric disorders. Cytogenet Genome Res 2006;113:271-278.
188. Umlauf D, Goto Y, Cao R, Cerqueira F, Wagschal A, Zhang Y, Feil R. Imprinting along the Kcnq1 domain on mouse chromosome 7 involves repressive histone methylation and recruitment of Polycomb group complexes. Nat Genet 2004; 36:1296-1300.
189. Van der Auwera I, D'Hooghe T. Superovulation of female mice delays embryonic and fetal development. Hum Reprod 2001;16:1237-1243.
190. van Dijk M, Mulders J, Konst A, Janssens B, van Roy F, Blankenstein M, Oudejans C. Differential downregulation of alphaT-catenin expression in placenta: trophoblast cell type-dependent imprinting of the CTNNA3 gene. Gene Expr Patterns 2004; 5:61-65.
191. Varmuza S, Mann M. Genomic imprinting-defusing the ovarian time bomb. Trends Genet 1994;10:118-123.
192. Vire E, Brenner C, Deplus R, Blanchon L, Fraga M, Didelot C, Morey L, Van Eynde A, Bernard D, Vanderwinden JM. et al. The Polycomb group protein EZH2 directly controls DNA methylation. Nature 2006;439:871-874.
193. Vlahovic M, Bulic-Jakus F, Juric-Lekic G, Fucic A, Maric S, Serman D. Changes in the placenta and in the rat embryo caused by the demethylating agent 5-azacytidine. Int J Dev Biol 1999;43:843-846.
194. Wagschal A, Feil R. Genomic imprinting in the placenta. Cytogenet Genome Res 2006; 113:90-98.
195. Wagschal A, Sutherland HG,Woodfine K, Henckel A, Chebli K, Schulz R, Oakey RJ, Bickmore WA, Feil R. G9a histone methyltransferase contributes to imprinting in the mouse placenta. Mol Cell Biol 2008;28:1104-1113.
196. Waldenstrom U, Engstrom AB, Hellberg D, Nilsson S. Low-oxygen compared with high-oxygen atmosphere in blastocyst culture, a prospective randomized study. Fertil Steril 2009;91:2461-2465.
197. Walsh C, Miller SJ, Flam F, Fisher RA, Ohlsson R. Paternally derived H19 is differentially expressed in malignant and nonmalignant trophoblast. Cancer Res 1995;55:1111-1116.
198. Wang J, Mager J, Chen Y, Schneider E, Cross JC, Nagy A, Magnuson T. Imprinted X inactivation maintained by a mouse Polycomb group gene. Nat Genet 2001; 28:371-375.
199. Wang J, Mager J, Schnedier E, Magnuson T. The mouse PcG gene eed is required for Hox gene repression and extraembryonic development. Mamm Genome 2002; 13:493-503.
200. Waterland RA, Jirtle RL. Transposable elements: targets for early nutritional effects on epigenetic gene regulation. Mol Cell Biol 2003;23:5293-5300.
201. Weaver JR, Sarkisian G, Krapp C, Mager J, Mann MR, Bartolomei MS. Domain-Specific Response of Imprinted Genes to Reduced DNMT1. Mol Cell Biol 2010;30:3916-3928.
202. Weber M, Schubeler D. Genomic patterns of DNA methylation: targets and function of an epigenetic mark. Curr Opin Cell Biol 2007;19:273-280.
203. Weisstein AE, Feldman MW, Spencer HG. Evolutionary genetic models of the ovarian time bomb hypothesis for the evolution of genomic imprinting. Genetics 2002;162:425-439.
204. Wolf JB, Cheverud JM, Roseman C, Hager R. Genome-wide analysis reveals a complex pattern of genomic imprinting in mice. PLoS Genet 2008;4:e1000091.
205. Wong NC, Novakovic B, Weinrich B, Dewi C, Andronikos R, Sibson M, Macrae F, Morley R, Pertile MD, Craig JM. et al. Methylation of the adenomatous polyposis coli (APC) gene in human placenta and hypermethylation in choriocarcinoma cells. Cancer Lett 2008;268:56-62.
206. Wood AJ, Oakey RJ. Genomic imprinting in mammals: emerging themes and established theories. PLoS Genet 2006;2:e147.
207. Wyatt SM, Kraus FT, Roh CR, Elchalal U, Nelson DM, Sadovsky Y. The correlation between sampling site and gene expression in the term human placenta. Placenta 2005;26:372-379.
208. Xue WC, Chan KY, Feng HC, Chiu PM, Ngan HY, Tsao SW, Cheung AN. Promoter hypermethylation of multiple genes in hydatidiform mole and choriocarcinoma. J Mol Diagn 2004;6:326-334.
209. Yang T, Adamson TE, Resnick JL, Leff S, Wevrick R, Francke U, Jenkins NA, Copeland NG, Brannan CI. A mouse model for Prader-Willi syndrome imprinting-centre mutations. Nat Genet 1998;19:25-31.
210. Yoder JA, Walsh CP, Bestor TH. Cytosine methylation and the ecology of intragenomic parasites. Trends Genet 1997;13:335-340.
211. Yokomine T, Kuroiwa A, Tanaka K, Tsudzuki M, Matsuda Y, Sasaki H. Sequence polymorphisms, allelic expression status and chromosome locations of the chicken IGF2 and MPR1 genes. Cytogenet Cell Genet 2001;93:109-113.
212. Yokomine T, Shirohzu H, Purbowasito W, Toyoda A, Iwama H, Ikeo K, Hori T, Mizuno S, Tsudzuki M, Matsuda Y. et al. Structural and functional analysis of a 0.5-Mb chicken region orthologous to the imprinted mammalian Ascl2/Mash2-Igf2-H19 region. Genome Res 2005;15:154-165.
213. Young LE, Fernandes K, McEvoy TG, Butterwith SC, Gutierrez CG, Carolan C, Broadbent PJ, Robinson JJ, Wilmut I, Sinclair KD. Epigenetic change in IGF2R is associated with fetal overgrowth after sheep embryo culture. Nat Genet 2001; 27:153-154.
214. Yu L, Chen M, Zhao D, Yi P, Lu L, Han J, Zheng X, Zhou Y, Li L. TheH19 gene imprinting in normal pregnancy and pre-eclampsia. Placenta 2009;30:443-447.
215. Zhang HJ, Siu MK, Wong ES, Wong KY, Li AS, Chan KY, Ngan HY, Cheung AN. Oct4 is epigenetically regulated by methylation in normal placenta and gestational trophoblastic disease. Placenta 2008;29:549-554.
216. Zhu XM, Han T, Sargent IL, Yin GW, Yao YQ. Differential expression profile of microRNAs in human placentas from preeclamptic pregnancies vs normal pregnancies. Am J Obstet Gynecol 2009;200:e661-667.